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Role of CRP in Leishmaniasis

  • Waliza Ansar
  • Shyamasree Ghosh
Chapter

Abstract

Different types of leishmaniasis are differentiated by range and complexity of clinical expressions ranging from asymptomatic infection to life-terrorizing illness. Visceral leishmaniasis (VL) is caused by an obligate intercellular parasite of the mononuclear phagocyte, Leishmania donovani, which causes a life-threatening disease. Leishmania during its stay in the human host have adapted to survive and proliferate in the host’s macrophages. The survival and proliferation of L. donovani in macrophages are largely due to the protection conferred by some family of glycosylinositol phospholipids or phosphoglycans on the cell surface or some secreted/expressed molecules of the host. C-reactive protein (CRP) is a prominent acute-phase protein of man. The serum concentration of CRP increases dramatically to nearly 10–1000-fold during inflammation following activation of hepatocytes by inflammatory cytokines. However, the function of CRP in inflammatory conditions and resistance to different infections is still less understood. CRP, a pattern recognition molecule, is present in host circulation. CRP binds to phosphorylcholine (PC) and some phosphorylated carbohydrates found on the surface of a number of microbes during their first entry into the mammalian host. Previously it was reported that CRP binds to the surface of L. donovani through their lipophosphoglycan (LPG) component and it increases the uptake of the parasite into host macrophages. Leishmania uses CRP to increase its infection without inducing any detrimental macrophage activation. The pathophysiology of different kinds of leishmaniasis was also abridged. CRP, being a phylogenetically conserved innate immune system recognition molecule, recognizes microbial determinants and components of damaged cells as an opsonin. CRP plays its effector function by activating the complement cascade and phagocytosis. A complete definition of the varied ligands used by CRP in recognizing the parasite is essential to understand its role in homeostasis and host defense. The main endeavor of this chapter is to unwind the functional significance of CRP in Leishmania infection, perpetuation, and survival in response to diverse host immune responses in the pathophysiology of its homeostatic mechanisms.

Keywords

Leishmania Lipophosphoglycan Phosphorylcholine Post-kala-azar dermal leishmaniasis Kala-azar 

References

  1. Alvar J, Cañavate C, Gutiérrez-Solar B, Jiménez M, Laguna F, López-Vélez R, Molina R, Moreno J (1997) Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin Microbiol Rev 10:298–319. [PMC free article] [PubMed]PubMedPubMedCentralGoogle Scholar
  2. Ansar W, Ghosh S (2013) C-reactive protein and the biology of disease. Immunol Res 56(1):131–142. doi: 10.1007/s12026-013-8384-0 PubMedCrossRefGoogle Scholar
  3. Ansar W, Habib SK, Roy S, Mandal C, Mandal C (2009a) Unraveling the C-reactive protein complement-cascade in destruction of red blood cells: potential pathological implications in Plasmodium falciparum malaria. Cell Physiol Biochem 23(1–3):175–190. doi: 10.1159/000204106. Epub 2009 Feb 18PubMedCrossRefGoogle Scholar
  4. Ansar W, Mukhopadhyay S, Habib SK, Basu S, Saha B, Sen AK, Mandal CN, Mandal C (2009b) Disease-associated glycosylated molecular variants of human C-reactive protein activate complement-mediated hemolysis of erythrocytes in tuberculosis and Indian visceral leishmaniasis. Glycoconj J 26(9):1151–69. doi: 10.1007/s10719-009-9236-y PubMedCrossRefGoogle Scholar
  5. Ansari NA, Sharma P, Salotra P (2007) Circulating nitric oxide and C-reactive protein levels in Indian kala azar patients: correlation with clinical outcome. Clin Immunol 122(3):343–348. Epub 2007 Jan 9PubMedCrossRefGoogle Scholar
  6. Ansari NA, Kumar R, Raj A, Salotra P (2008) Elevated levels of IgG3 and IgG4 subclass in paediatric cases of kala azar. Parasite Immunol 30(8):403–409. doi: 10.1111/j.1365-3024.2008.01036.x PubMedCrossRefGoogle Scholar
  7. Arik Yilmaz E, Tanir G, Tuygun N, Taylan Ozkan A (2009) Visceral leishmaniasis in 13 pediatric patients in Turkey: treatment experience. Turkiye Parazitol Derg 33(4):259–262PubMedGoogle Scholar
  8. Ballou SP, Lozanski G (1992) Induction of inflammatory cytokine release from cultured human monocytes by C-reactive protein. Cytokine 4:361–368PubMedCrossRefGoogle Scholar
  9. Bandyopadhyay SM, Mandal C (2008) Targeting glycoproteins or glycolipids and their metabolic pathways for antiparasite therapy. Adv Exp Med Biol 625:87–102PubMedCrossRefGoogle Scholar
  10. Bandyopadhyay S, Chatterjee M, Das T, Bandyopadhyay S, Sundar S, Mandal C (2004) Antibodies directed against O-acetylated sialoglycoconjugates accelerate complement activation in Leishmania donovani promastigotes. J Infect Dis 190(11):2010–2019, Epub 2004 Nov 3PubMedCrossRefGoogle Scholar
  11. Bee A, Culley FJ, Alkhalife IS, Bodman-Smith KB, Raynes JG, Bates PA (2001) Transformation of Leishmania mexicana metacyclic promastigotes to amastigote-like forms mediated by binding of human C-reactive protein. Parasitology 122:521–529PubMedCrossRefGoogle Scholar
  12. Bern C, Haque R, Chowdhury R, Ali M, Kurkjian KM, Vaz L, Amann J, Wahed MA, Wagatsuma Y, Breiman RF, Williamson J, Secor WE, Maguire JH (2007) The epidemiology of visceral leishmaniasis and asymptomatic leishmanial infection in a highly endemic Bangladeshi village. Am J Trop Med Hyg 76(5):909–914PubMedGoogle Scholar
  13. Beverley SM, Turco SJ (1998) Lipophosphoglycan (LPG) and the identification of virulence genes in the protozoan parasite Leishmania. Trends Microbiol 6:35–40PubMedCrossRefGoogle Scholar
  14. Bharadwaj D, Stein MP, Volzer M, Mold C, Du Clos TW (1999) The major receptor for C-reactive protein on leukocytes is Fcγ receptor II. J Exp Med 190:585–590PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bharadwaj D, Mold C, Markham E, Du Clos TW (2001) Serum amyloid P component binds to Fc gamma receptors and opsonizes particles for phagocytosis. J Immunol 166:6735–6741PubMedCrossRefGoogle Scholar
  16. Bodman-smith KB, Melendez AJ, Campbell I, Harrison PT, Allen JM, Raynes JG (2002a) C-reactive protein-mediated phagocytosis and phospholipase D signalling through the high-affinity receptor for immunoglobulin G (FcγRI). Immunology 107:252–260PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bodman-Smith KB, Mbuchi M, Culley FJ, Bates PA, Raynes JG (2002b) C-reactive protein-mediated phagocytosis of Leishmania donovani promastigotes does not alter parasite survival or macrophage responses. Parasite Immunol 24(9–10):447–454PubMedCrossRefGoogle Scholar
  18. Bora D (1999) Epidemiology of visceral leishmaniasis in India. Natl Med J India 12(2):62–68PubMedGoogle Scholar
  19. Bouree P, Botterel F, Lancon A (2000) Study of protein profile in the visceral leishmaniasis. J Egypt Soc Parasitol 30(3):885–893PubMedGoogle Scholar
  20. Bredt DS, Synder SH (1994) Nitric oxide: a physiologic messenger molecule. Ann Rev Biochem 63:175–195PubMedCrossRefGoogle Scholar
  21. Chakraborty R, Chakraborty P, Basu MK (1998) Macrophage mannosyl fucosyl receptor: its role in invasion of virulent and avirulent L. donovani promastigotes. Biosci Rep 18(3):129–142PubMedCrossRefGoogle Scholar
  22. Chang KP (1981) Leishmania donovani-macrophage binding mediated by surface glycoproteins/antigens: characterization in vitro by a radioisotopic assay. Mol Biochem Parasitol 4(1–2):67–76PubMedCrossRefGoogle Scholar
  23. Channon JY, Roberts MB, Blackwell JM (1984) A study of the differential respiratory burst activity elicited by promastigotes and amastigotes of Leishmania donovani in murine resident peritoneal macrophages. Immunology 53:345–355PubMedPubMedCentralGoogle Scholar
  24. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol 5(11):873–882PubMedCrossRefGoogle Scholar
  25. Chatterjee M, Chava AK, Kohla G, Pal S, Merling A, Hinderlich S, Unger U, Strasser P, Gerwig GJ, Kamerling JP, Vlasak R, Crocker PR, Schauer R, Schwartz-Albiez R, Mandal C (2003) Identification and characterization of adsorbed serum sialoglycans on Leishmania donovani promastigotes. Glycobiology 13:351–361PubMedCrossRefGoogle Scholar
  26. Chava AK, Chatterjee M, Gerwig GJ, Kamerling JP, Mandal C (2004) Identification of sialic acids on Leishmania donovani amastigotes. Biol Chem 385:59–66PubMedCrossRefGoogle Scholar
  27. Chava AK, Chatterjee M, Mandal C (2005) O-acetyl sialic acids in parasitic diseases. In: Yarema KJ (ed) Handbook of carbohydrate engineering. Chapter 3. Taylor and Francis Group, book division, Florida, pp 71–86 and references thereinGoogle Scholar
  28. Culley FJ, Thomson M, Raynes JG (1997) C-reactive protein increases C3 deposition on Leishmania donovani promastigotes in human serum. Biochem Soc Trans 25(2):286SPubMedCrossRefGoogle Scholar
  29. Culley FJ, Harris RA, Kaye PM, McAdam PWJ, Raynes JG (1996) C-reactive protein binds to a novel ligand on Leishmania donovani and increases uptake into human macrophages. J Immunol 156(12):4691–4696PubMedGoogle Scholar
  30. Culley FJ, Bodman-Smith KB, Ferguson MAJ, Nikolaev AV, Shantilal N, Raynes JG (2000) C-reactive protein binds to phosphorylated carbohydrates. Glycobiology 10(1):59–65, And references thereinPubMedCrossRefGoogle Scholar
  31. Das T, Sen A, Kempf T, Pramanik SR, Mandal C, Mandal C (2003) Induction of glycosylation in human C-reactive protein under different pathological conditions. Biochem J 373(Pt 2):345–355PubMedPubMedCentralCrossRefGoogle Scholar
  32. Das T, Mandal C, Mandal C (2004a) Variations in binding characteristics of glycosylated human C-reactive proteins in different pathological conditions. Glycoconj J 20(9):537–543PubMedCrossRefGoogle Scholar
  33. Desjeux P (1999) Global control and Leishmania HIV co-infection. Clin Dermatol 17:317–325. [PubMed]PubMedCrossRefGoogle Scholar
  34. Desjeux P (2001) The increase in risk factors for leishmaniasis worldwide. Trans R Soc Trop Med Hyg 95:239–243. [PubMed]PubMedCrossRefGoogle Scholar
  35. Dortay H, Schmöckel SM, Fettke J, Mueller-Roeber B (2011) Expression of human c-reactive protein in different systems and its purification from Leishmania tarentolae. Protein Expr Purif 78(1):55–60. doi: 10.1016/j.pep.2011.03.010. Epub 2011 Apr 1PubMedCrossRefGoogle Scholar
  36. Du Clos TW (2000) Function of C-reactive protein. Ann Med 32:274–278PubMedCrossRefGoogle Scholar
  37. Galve-de Rochemonteix B, Wiktorowicz K, Kushner I, Dayer JM (1993) C-reactive protein increases production of IL-1 alpha, IL-1 beta, and TNF-alpha, and expression of mRNA by human alveolar macrophages. J Leukoc Biol 53:439–445PubMedGoogle Scholar
  38. Ganguly S, Das NK, Barbhuiya JN, Chatterjee M (2010) Post-kala-azar dermal leishmaniasis – an overview. Int J Dermatol 49(8):921–931. doi: 10.1111/j.1365-4632.2010.04558.x PubMedCrossRefGoogle Scholar
  39. Gardinassi LG, Dotz V, Hipgrave Ederveen A, de Almeida RP, Nery Costa CH, Costa DL, de Jesus AR, Mayboroda OA, Garcia GR, Wuhrer M, de Miranda Santos IK (2014) Clinical severity of visceral leishmaniasis is associated with changes in immunoglobulin g fc N-glycosylation. MBio 5(6):e01844. doi: 10.1128/mBio.01844-14 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gasim S, Theander TG, ElHassan AM (2000) High levels of C-reactive protein in the peripheral blood during visceral leishmaniasis predict subsequent development of post kala-azar dermal leishmaniasis. Acta Trop 75(1):35–38PubMedCrossRefGoogle Scholar
  41. Ghalib HW, Whittle JA, Kubin M et al (1995a) IL −12 enhances Th1-type responses in human Leishmania donovani infections. J Immunol 154:4623–4629PubMedGoogle Scholar
  42. Ghalib HW, Piuvezam MR, Skeiky YA et al (1995b) Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 92:324–329CrossRefGoogle Scholar
  43. Gotschlich EC, Edelman GM (1967) Binding properties and specificity of C-reactive protein. Proc Natl Acad Sci U S A 57:706–712PubMedPubMedCentralCrossRefGoogle Scholar
  44. Guy RA, Bolosevic M (1993) Comparson of receptors required for entry of Leishmania major amastigotes by macrophages. Infect Immunol 61:1553–1558Google Scholar
  45. Herwaldt BL (2001) Leishmaniasis. In: Braunwald E, Fauci AS, Kasper DL, Hauser SL, Longo DL, Jameson JL (eds) Harrison's principles of internal medicine. McGraw Hill Companies, Inc., New York, pp 1213–1218Google Scholar
  46. Ibba F, Rossi G, Meazzi S, Giordano A, Paltrinieri S (2014) Serum concentration of high density lipoproteins (HDLs) in leishmaniotic dogs. Res Vet Sci 98:89–91. doi: 10.1016/j.rvsc.2014.11.011. pii: S0034-5288(14)00312-9PubMedCrossRefGoogle Scholar
  47. Kaplan MH, Volanakis JE (1974) Interactions of C-reactive protein complexes with the complement system, I: consumption of human complement associated with the reaction of C-reactive protein with pneumococcal C-polysaccharide and with the choline phosphatides, lecithin and sphingomyelin. J Immunol 112:2135–2147PubMedGoogle Scholar
  48. Kaul P, Malla N, Kaur S, Mahajan RC, Ganguly NK (2000) Evaluation of a 200-kDa amastigote-specific antigen of L. donovani by enzyme-linked immunosorbent assay (ELISA) for the diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg 94:173–175PubMedCrossRefGoogle Scholar
  49. Kausalya S, Kaur S, Malla N, Ganguly NK, Mahajan RC (1996) Microbicidal mechanisms of liver macrophages in experimental visceral leishmaniasis. APMIS 104:171–175PubMedCrossRefGoogle Scholar
  50. Kelm S, Schauer R (1997) Sialic acids in molecular and cellular interactions. Int Rev Cytol 175:137–240PubMedCrossRefGoogle Scholar
  51. Khorvash F, Naeini AE, Behjati M, Abdi F (2011) Visceral leishmaniasis in a patient with cutaneous lesions, negative Leishman-Donovan bodies and immunological test: A case report. J Res Med Sci 16(11):1507–1510PubMedPubMedCentralGoogle Scholar
  52. Kima PE, Constant SL, Hannum L, Colmenares M, Lee KS, Haberman AM, Shlomchik MJ, McMahon-Pratt D (2000) Internalisation of Leishmania mexicana complex amastigotes via the Fc receptor is required to sustain infection in murine cutaneous leishmaniasis. J Exp Med 191:1063–1067PubMedPubMedCentralCrossRefGoogle Scholar
  53. Leishman WB (2006) On the possibility of the occurrence of trypanosomiasis in India. 1903. Indian J Med Res 123(3):1252–1254; discussion 79PubMedGoogle Scholar
  54. Lodge R, Diallo TO, Descoteaux A (2006) Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell Microbiol 8:1922–1931PubMedCrossRefGoogle Scholar
  55. Malla N, Mahajan RC (2006) Pathophysiology of visceral leishmaniasis – some recent concepts. Indian J Med Res 123:267–274PubMedGoogle Scholar
  56. Marnell LL, Mold C, Volzer MA, Burlingame RW, Du Clos TW (1995) C-reactive protein binds to FcYRI in transfected COS cells. J Immunol 155:2185–2193PubMedGoogle Scholar
  57. Marnell L, Mold C, Du Clos TW (2005) C-reactive protein: ligands, receptors and role in inflammation. Clin Immunol 117:104–111PubMedCrossRefGoogle Scholar
  58. Marsden PD, Jones TC (1985) Clinical manifestations, diagnosis and treatment of leishmaniasis. In: Chang KP, Bray RS (eds) Leishmaniasis. Elsevier Science Publishers, Amsterdam, pp 183–198Google Scholar
  59. Martinez-Subiela S, Strauss-Ayali D, Cerón JJ, Baneth G (2011) Acute phase protein response in experimental canine leishmaniasis. Vet Parasitol 180(3–4):197–202. doi: 10.1016/j.vetpar.2011.03.032. Epub 2011 Mar 31PubMedCrossRefGoogle Scholar
  60. Martínez-Subiela S, García-Martínez JD, Tvarijonaviciute A, Tecles F, Caldin M, Bernal LJ, Cerón JJ (2013) Urinary C reactive protein levels in dogs with leishmaniasis at different stages of renal damage. Res Vet Sci 95(3):924–929. doi: 10.1016/j.rvsc.2013.07.002. Epub 2013 Aug 6PubMedCrossRefGoogle Scholar
  61. McConville MJ, Turco SJ, Ferguson MA, Sacks DL (1992) Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J 11(10):3593–3600. Biomedica. 2002 Jun;22(2):167–177Google Scholar
  62. Mold C, Du Clos TW (2006) C-reactive protein increases cytokine responses to Streptococcus pneumoniae through interactions with Fc gamma receptors. J Immunol 176(12):7598–7604PubMedCrossRefGoogle Scholar
  63. Mondal D, Khan MG (2011) Recent advances in post-kala-azar dermal leishmaniasis. Curr Opin Infect Dis 24(5):418–422. doi: 10.1097/QCO.0b013e32834a8ba1 PubMedCrossRefGoogle Scholar
  64. Mortensen RF, Zhong W (2000) Regulation of phagocytic leukocyte activities by C reactive protein. J Leukoc Biol 67:495–500PubMedGoogle Scholar
  65. Mortensen RF, Osmand AP, Lint TF, Gewurz H (1976) Interaction of C-reactive protein with lymphocytes and monocytes: complement-dependent adherence and phagocytosis. J Immunol 117(3):774–781PubMedGoogle Scholar
  66. Mosser DM, Brittingham A (1997) Leishmania, macrophages and complement: a tale of subversion and expression. Parasitology 115:S9–S23PubMedCrossRefGoogle Scholar
  67. Mosser DM, Edelson PJ (1984) Activation of the alternative complement pathway by Leishmania promastigotes; parasite lysis and attachment to macrophages. J Immunol 132(3):1501–1505PubMedGoogle Scholar
  68. Mosser DM, Rosenthal LA (1997) Leishmania-macrophage interactions: multiple receptors, multiple ligands and diverse cellular responses. Semin Cell Biol 4:315–322CrossRefGoogle Scholar
  69. Mukhopadhyay S, Mandal C (2006) Glycobiology of Leishmania donovani. Indian J Med Res 123:203–220PubMedGoogle Scholar
  70. Mukhopadhyay D, Dalton JE, Kaye PM, Chatterjee M (2014) Post kala-azar dermal leishmaniasis: an unresolved mystery. Trends Parasitol 30(2):65–74. doi: 10.1016/j.pt.2013.12.004 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Muskus CE, Marín VM (2002) Metacyclogenesis: a basic process in the biology of Leishmania. Biomedica 22(2):167–177PubMedCrossRefGoogle Scholar
  72. Oliveira EB, Gotschlich EC, Liu T-Y (1979) Primary structure of human C-reactive protein. J Biol Chem 254(2):489–502PubMedGoogle Scholar
  73. Oztoprak N, Aydemir H, Pişkin N, Seremet Keskin A, Araslı M, Gökmen A, Celebi G, Külekçi Uğur A, Taylan Özkan A (2010) An adult case of visceral leishmaniasis in a province of Black-Sea region, Turkey. Mikrobiyol Bul 44(4):671–677PubMedGoogle Scholar
  74. Pal S, Chatterjee M, Bhattacharya DK, Bandhyopadhyay S, Mandal C (2000) Identification and purification of cytolytic antibodies directed against O-acetylated sialic acid in childhood acute lymphoblastic leukemia. Glycobiology 10(6):539–549PubMedCrossRefGoogle Scholar
  75. Paltrinieri S, Ravicini S, Rossi G, Roura X (2010) Serum concentrations of the derivatives of reactive oxygen metabolites (d-ROMs) in dogs with leishmaniosis. Vet J 186(3):393–395. doi: 10.1016/j.tvjl.2009.08.019. Epub 2009 Sep 15PubMedCrossRefGoogle Scholar
  76. Peters C, Aebischer A, Stiehorf YD, Fuchs M, Overath P (1995) The role of macrophage receptors in adhesion and uptake of Leishmania Mexicana amastigotes. J Cell Sci 108:3715–3724PubMedGoogle Scholar
  77. Pritchard DG, Volanakis JE (1985) Slutsky GM and Greenblatt CL C-reactive protein binds leishmanial excreted factors. Proc Soc Exp Biol Med 178(3):500–503PubMedCrossRefGoogle Scholar
  78. Proudfoot L, O’Donnell CA, Liew FY (1995) Glycoinositolphospholipids of Leishmania major inhibit nitric oxide synthesis and reduce leishmaniacidal activity in murine macrophages. Eur J Immunol 25:745–750PubMedCrossRefGoogle Scholar
  79. Ratnam S, Mookerjea S (1998) The regulation of superoxide generation and nitric oxide synthesis by C-reactive protein. Immunology 94:560–568PubMedPubMedCentralCrossRefGoogle Scholar
  80. Ready PD (2014) Epidemiology of visceral leishmaniasis. Clin Epidemiol 6:147–154. doi: 10.2147/CLEP.S44267. eCollection 2014PubMedPubMedCentralCrossRefGoogle Scholar
  81. Remaley AT, Kuhns DB, Basford RE, Glew RH, Kaplan SS (1984) Leishmanial phosphatase blocks neutrophil O-2 production. J Biol Chem 259(18):11173–11175PubMedGoogle Scholar
  82. Rittig MG, Bogdan C (2000) Leishmania–host-cell interaction: complexities and alternative views. Parasitol Today 16:292–297PubMedCrossRefGoogle Scholar
  83. Rivzi FS, Ouaissi MA, Marty B, Santoro F, Capron A (1988) The major surface protein of Leishmania promastigotes is a fibronectin -like molecule. Eur J Immunol 18:473–476CrossRefGoogle Scholar
  84. Rossi G, Ibba F, Meazzi S, Giordano A, Paltrinieri S (2014) Paraoxonase activity as a tool for clinical monitoring of dogs treated for canine leishmaniasis. Vet J 199(1):143–149. doi: 10.1016/j.tvjl.2013.10.007. Epub 2013 Oct 11PubMedCrossRefGoogle Scholar
  85. Sharma U, Singh S (2009) Immunobiology of leishmaniasis. Indian J Exp Biol 47:412–423PubMedGoogle Scholar
  86. Sharma V, Chatterjee M, Mandal C, Sen S, Basu D (1998) Rapid diagnosis of Indian visceral leishmaniasis using achatinin H, a 9-O-acetylated sialic acid binding lectin. Am J Trop Med Hyg 58:551–554PubMedGoogle Scholar
  87. Shukla AK, Schauer R (1982) Fluorimetric determination of unsubstituted and 9(8)-O-acetylated sialic acids in erythrocyte membranes. Hoppe Seylers Z Physiol Chem 363(3):255–262PubMedCrossRefGoogle Scholar
  88. Silverstein SC (1977) Endocytic uptake of particles by mononuclear phagocytes and the penetration of obligate intracellular parasites. Am J Trop Med Hyg 26:161–169PubMedGoogle Scholar
  89. Singh S, Sharma U, Mishra J (2011) Post-kala-azar dermal leishmaniasis: recent developments. Int J Dermatol 50(9):1099–1108. doi: 10.1111/j.1365-4632.2011.04925.x PubMedCrossRefGoogle Scholar
  90. Sundar S, Rai M (2002) Advances in the treatment of leishmaniasis. Curr Opin Infect Dis 15(6):593–598PubMedCrossRefGoogle Scholar
  91. Sundar S, Singh A, Chakravarty J, Rai M (2015) Efficacy and safety of miltefosine in treatment of post-kala-azar dermal leishmaniasis. ScientificWorldJournal 2015:414378. doi: 10.1155/2015/414378. Epub 2015 Jan 1PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sunder S, Pai K, Sahu M, Kumar V, Murray HW (2002) Immunochromatographic strip-test detection of anti-K39 antibody in Indian visceral leishmaniasis. Ann Trop Med Parasitol 96:19–23CrossRefGoogle Scholar
  93. Suresh MV, Singh SK, Ferguson DA Jr, Agrawal A (2007) Human C-reactive protein protects mice from Streptococcus pneumoniae infection without binding to pneumococcal C-polysaccharide. J Immunol 178(2):1158–1163PubMedPubMedCentralCrossRefGoogle Scholar
  94. Szalai AJ, McCrory MA (2002) Varied biologic functions of C-reactive protein: lessons learned from transgenic mice. Immunol Res 26(1–3):279–287PubMedCrossRefGoogle Scholar
  95. Szalai AJ, Briles DE, Volanakis JE (1995) Human C-reactive protein is protective against fatal Streptococcus pneumoniae infection in transgenic mice. J Immunol 155(5):2557–2563PubMedGoogle Scholar
  96. Szalai AJ, Alarcón GS, Calvo-Alén J, Toloza SM, McCrory MA, Edberg JC, McGwin G Jr, Bastian HM, Fessler BJ, Vilá LM, Kimberly RP, Reveille JD (2005a) Systemic lupus erythematosus in a multiethnic US Cohort (LUMINA). XXX: association between C-reactive protein (CRP) gene polymorphisms and vascular events. Rheumatology (Oxford) 44(7):864–868. Epub 2005 Mar 29CrossRefGoogle Scholar
  97. Szalai AJ, Wu J, Lange EM, McCrory MA, Langefeld CD, Williams A, Zakharkin SO, George V, Allison DB, Cooper GS, Xie F, Fan Z, Edberg JC, Kimberly RP (2005b) Single-nucleotide polymorphisms in the C-reactive protein (CRP) gene promoter that affect transcription factor binding, alter transcriptional activity, and associate with differences in baseline serum CRP level. J Mol Med (Berl) 83(6):440–447. Epub 2005 Mar 19CrossRefGoogle Scholar
  98. Thakur CP (2000) Socioeconomics of visceral leishmaniasis in Bihar (India). Trans R Soc Trop Med Hyg 94:156–157. [PubMed]PubMedCrossRefGoogle Scholar
  99. Thomas-Rudolph D, Du Clos TW, Snapper CM, Mold C (2007) C-reactive protein enhances immunity to Streptococcus pneumoniae by targeting uptake to Fc gamma R on dendritic cells. J Immunol 178(11):7283–7291PubMedCrossRefGoogle Scholar
  100. Varki A (2008) Multiple changes in sialic acid biology during human evolution. Glycoconj J 26:231–245PubMedCrossRefGoogle Scholar
  101. Volanakis JE (2001) Human C-reactive protein: expression, structure, and function. Mol Immunol 38:189–197PubMedCrossRefGoogle Scholar
  102. Wasunna KM, Raynes JG, Were JB, Muigai R, Sherwood J, Gachihi G, Carpenter L, McAdam KP (1995) Acute phase protein concentrations predict parasite clearance rate during therapy for visceral leishmaniasis. Trans R Soc Trop Med Hyg 89(6):678–681PubMedCrossRefGoogle Scholar
  103. Wilson ME, Pearson RD (1986) Evidence that Leishmania donovani utilises a mannose receptor on human mononuclear phagocytes to establish intracellular infection. J Immunol 136:4681–4688PubMedGoogle Scholar
  104. Wilson ME, Pearson RD (1988) Roles of CR3 and mannose receptors in the attachment and ingestion of Leishmania donovani by human mononuclear phagocytes. Infect Immun 56:363–369PubMedPubMedCentralGoogle Scholar
  105. Wilson ME, Sandor M, Blum AM et al (1996) Local suppression of IFN-gamma in hepatic granulomas correlates with tissue-specific replication of Leishmania chagasi. J Immunol 156:2231–2239PubMedGoogle Scholar
  106. World Health Organization (1995) Report on the consultative meeting on Leishmania/HIV Co-infection, Rome, 6–7 September 1994. Document WHO/LEISH/ 95.35. WHO, GenevaGoogle Scholar
  107. World Health Organization Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control of Leishmaniases, Geneva, March 22–26, 2010. World Health Organ Tech Rep Ser 949:1–186Google Scholar
  108. Zijlstra EE, Musa AM, Khalil EAG, El Hassan IM, El-Hassan AM (2003) Post-kala-azar dermal leishmaniasis. Lancet Infect Dis 3(2):87–98. doi: 10.1016/s1473-3099(03)00517-6 PubMedCrossRefGoogle Scholar

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© Springer India 2016

Authors and Affiliations

  • Waliza Ansar
    • 1
  • Shyamasree Ghosh
    • 2
  1. 1.Department of ZoologyBehala CollegeKolkataIndia
  2. 2.National Institute of Science EducationSchool of Biological SciencesBhubaneswarIndia

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